Norovirus triggered microbiota-driven mucosal inflammation in interleukin 10-deficient mice

Inflammatory Bowel Diseases

Volumn 20, Issue 3, 2014, Pages 431-443

  Basic, Marijana ^a   Keubler, Lydia M ^a   Buettner, Manuela ^a   Achard, Marcel ^a,b   Breves, Gerhard ^c   Schröder, Bernd ^c   Smoczek, Anna ^a   Jörns, Anne ^a   Wedekind, Dirk ^a   Zschemisch, Nils H ^a   Günther, Claudia ^d   Neumann, Detlef ^a   Lienenklaus, Stefan ^e   Weiss, Siegfried ^e   Hornef, Mathias W ^a   Mähler, Michael ^b   Bleich, André ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b BioDoc   (Germany)

^c UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^e HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

IBD; Il102 2; Intestinal barrier; MNV

Indexed keywords

INTERLEUKIN 10; MANNITOL; TIGHT JUNCTION PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; EPITHELIUM CELL; GENE EXPRESSION; GENE TECHNOLOGY; HISTOPATHOLOGY; IMMUNOHISTOLOGY; INTESTINE FLORA; INTESTINE MUCOSA; MOUSE; MUCOSA INFLAMMATION; NICK END LABELING; NONHUMAN; NOROVIRUS; NOROVIRUS INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIGHT JUNCTION; TRANSGENE; WILD TYPE;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CALICIVIRIDAE INFECTIONS; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; INFLAMMATION; INTERLEUKIN-10; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROBIOTA; MUCOSITIS; NOROVIRUS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84897144989     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/01.MIB.0000441346.86827.ed     Document Type: Article

References (55)

1. Turner Jr. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol. 2009;9:799-809.
2. Kaser A, Zeissig S, Blumberg RS. Inflammatory bowel disease. Annu Rev Immunol. 2010;28:573-621.
3. Packey CD, Sartor RB. Commensal bacteria, traditional and opportunistic pathogens, dysbiosis and bacterial killing in inflammatory bowel diseases. Curr Opin Infect Dis. 2009;22:292-301.
4. Hsu CC, Wobus CE, Steffen EK, et al. Development of a microspherebased serologic multiplexed fluorescent immunoassay and a reverse transcriptase PCR assay to detect murine norovirus 1 infection in mice. Clin Diagn Lab Immunol. 2005;12:1145-1151.
5. Mähler M, Köhl W. A serological survey to evaluate contemporary prevalence of viral agents and Mycoplasma pulmonis in laboratory mice and rats in western Europe. Lab Anim (NY). 2009;38:161-165.
6. Pritchett-Corning KR, Cosentino J, Clifford CB. Contemporary prevalence of infectious agents in laboratory mice and rats. Lab Anim. 2009; 43:165-173.
7. Fankhauser RL, Noel JS, Monroe SS, et al. Molecular epidemiology of "Norwalk-like viruses" in outbreaks of gastroenteritis in the United States. J Infect Dis. 1998;178:1571-1578.
8. Karst SM. Pathogenesis of noroviruses, emerging RNA viruses. Viruses. 2010;2:748-781.
9. Karst SM, Wobus CE, Lay M, et al. STAT1-dependent innate immunity to a Norwalk-like virus. Science. 2003;299:1575-1578.
10. Mumphrey SM, Changotra H, Moore TN, et al. Murine norovirus 1 infection is associated with histopathological changes in immunocompetent hosts, but clinical disease is prevented by STAT1-dependent interferon responses. J Virol. 2007;81:3251-3263.
11. Wobus CE, Karst SM, Thackray LB, et al. Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol. 2004;2:e432.
12. Cadwell K, Patel KK, Maloney NS, et al. Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine. Cell. 2010;141:1135-1145.
13. Lencioni KC, Seamons A, Treuting PM, et al. Murine norovirus: an intercurrent variable in a mouse model of bacteria-induced inflammatory bowel disease. Comp Med. 2008;58:522-533.
14. Higgins PD, Johnson LA, Sauder K, et al. Transient or persistent norovirus infection does not alter the pathology of Salmonella typhimurium induced intestinal inflammation and fibrosis in mice. Comp Immunol Microbiol Infect Dis. 2011;34:247-257.
15. Nicklas W, Baneux P, Boot R, et al. Recommendations for the health monitoring of rodent and rabbit colonies in breeding and experimental units. Lab Anim. 2002;36:20-42.
16. Cox C, Cao S, Lu Y. Enhanced detection and study of murine norovirus-1 using a more efficient microglial cell line. Virol J. 2009;6:196.
17. Lienenklaus S, Cornitescu M, Zietara N, et al. Novel reporter mouse reveals constitutive and inflammatory expression of IFN-beta in vivo. J Immunol. 2009;183:3229-3236.
18. Solodova E, Jablonska J, Weiss S, et al. Production of IFN-beta during Listeria monocytogenes infection is restricted to monocyte/macrophage lineage. PloS One. 2011;6:e18543.
19. Bens M, Bogdanova A, Cluzeaud F, et al. Transimmortalized mouse intestinal cells (m-ICc12) that maintain a crypt phenotype. Am J Physiol. 1996;270:C1666-C1674.
20. Hornef MW, Frisan T, Vandewalle A, et al. Toll-like receptor 4 resides in the Golgi apparatus and colocalizes with internalized lipopolysaccharide in intestinal epithelial cells. J Exp Med. 2002;195:559-570.
21. Janus LM, Smoczek A, Jörns A, et al. Presence of Minute virus of mice in immunocompetent mice despite the onset of host immunity. Vet Microbiol. 2010;146:51-58.
22. Baert L, Wobus CE, Van Coillie E, et al. Detection of murine norovirus 1 by using plaque assay, transfection assay, and real-time reverse transcription-PCR before and after heat exposure. Appl Environ Microbiol. 2008;74: 543-546.
23. Bleich A, Mähler M, Most C, et al. Refined histopathologic scoring system improves power to detect colitis QTL in mice. Mamm Genome. 2004; 15:865-871.
24. Bleich A, Janus LM, Smoczek A, et al. CpG motifs of bacterial DNA exert protective effects in mouse models of IBD by antigen-independent tolerance induction. Gastroenterology. 2009;136:278-287.
25. Neumann D, Tschernig T, Popa D, et al. Injection of IL-12-and IL-18-encoding plasmids ameliorates the autoimmune pathology of MRL/Mp-Tnfrsf6lpr mice: synergistic effect on autoimmune symptoms. Int Immunol. 2006;18:1779-1787.
26. Bleich EM, Leonhard-Marek S, Beyerbach M, et al. Characterisation of chloride currents across the proximal colon in CftrTgH(neoim)1Hgu congenic mice. J Comp Physiol B. 2007;177:61-73.
27. Toth B, Leonhard-Marek S, Hedrich HJ, et al. Characterisation of electrogenic nutrient absorption in the Cftr TgH(neoim)Hgu mouse model. J Comp Physiol B. 2008;178:705-712.
28. Schroeder B, Duncker S, Barth S, et al. Preventive effects of the probiotic Escherichia coli strain Nissle 1917 on acute secretory diarrhea in a pig model of intestinal infection. Dig Dis Sci. 2006;51:724-731.
29. Schultz SG, Zalusky R. Ion transport in isolated rabbit ileum. I. Shortcircuit current and Na Fluxes. J Gen Physiol. 1964;47:567-584.
30. Jörns A, Gunther A, Hedrich HJ, et al. Immune cell infiltration, cytokine expression, and beta-cell apoptosis during the development of type 1 diabetes in the spontaneously diabetic LEW.1AR1/Ztm-iddm rat. Diabetes. 2005;54:2041-2052.
31. Souza M, Azevedo MS, Jung K, et al. Pathogenesis and immune responses in gnotobiotic calves after infection with the genogroup II.4-HS66 strain of human norovirus. J Virol. 2008;82:1777-1786.
32. Hsu CC, Riley LK, Wills HM, et al. Persistent infection with and serologic cross-reactivity of three novel murine noroviruses. Comp Med. 2006;56:247-251.
33. Atmar RL, Opekun AR, Gilger MA, et al. Norwalk virus shedding after experimental human infection. Emerg Infect Dis. 2008;14:1553-1557.
34. Duizer E, Schwab KJ, Neill FH, et al. Laboratory efforts to cultivate noroviruses. J Gen Virol. 2004;85:79-87.
35. Khan RR, Lawson AD, Minnich LL, et al. Gastrointestinal norovirus infection associated with exacerbation of inflammatory bowel disease. J Pediatr Gastroenterol Nutr. 2009;48:328-333.
36. Rahbar A, Bostrom L, Lagerstedt U, et al. Evidence of active cytomegalovirus infection and increased production of IL-6 in tissue specimens obtained from patients with inflammatory bowel diseases. Inflamm Bowel Dis. 2003;9:154-161.
37. Yanai H, Shimizu N, Nagasaki S, et al. Epstein-Barr virus infection of the colon with inflammatory bowel disease. Am J Gastroenterol. 1999;94:1582-1586.
38. Perdue KA, Green KY, Copeland M, et al. Naturally occurring murine norovirus infection in a large research institution. J Am Assoc Lab Anim Sci. 2007;46:39-45.
39. Ward JM, Wobus CE, Thackray LB, et al. Pathology of immunodeficient mice with naturally occurring murine norovirus infection. Toxicol Pathol. 2006;34:708-715.
40. Cooney R, Baker J, Brain O, et al. NOD2 stimulation induces autophagy in dendritic cells influencing bacterial handling and antigen presentation. Nat Med. 2010;16:90-97.
41. Farmer MA, Sundberg JP, Bristol IJ, et al. A major quantitative trait locus on chromosome 3 controls colitis severity in IL-10-deficient mice. Proc Natl Acad Sci U S A. 2001;98:13820-13825.
42. Sellon RK, Tonkonogy S, Schultz M, et al. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun. 1998; 66:5224-5231.
43. Troeger H, Loddenkemper C, Schneider T, et al. Structural and functional changes of the duodenum in human norovirus infection. Gut. 2009;58: 1070-1077.
44. Gitter AH, Bendfeldt K, Schulzke JD, et al. Leaks in the epithelial barrier caused by spontaneous and TNF-alpha-induced single-cell apoptosis. FASEB J. 2000;14:1749-1753.
45. Cheetham S, Souza M, Meulia T, et al. Pathogenesis of a genogroup II human norovirus in gnotobiotic pigs. J Virol. 2006;80:10372-10381.
46. Bok K, Prikhodko VG, Green KY, et al. Apoptosis in murine norovirusinfected RAW264.7 cells is associated with downregulation of survivin. J Virol. 2009;83:3647-3656.
47. Furman LM, Maaty WS, Petersen LK, et al. Cysteine protease activation and apoptosis in Murine norovirus infection. Virol J. 2009;6:139.
48. Amasheh S, Fromm M, Gunzel D. Claudins of intestine and nephron-a correlation of molecular tight junction structure and barrier function. Acta Physiol (Oxf). 2011;201:133-140.
49. Burgel N, Bojarski C, Mankertz J, et al. Mechanisms of diarrhea in collagenous colitis. Gastroenterology. 2002;123:433-443.
50. Zeissig S, Burgel N, Gunzel D, et al. Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn's disease. Gut. 2007;56: 61-72.
51. Prasad S, Mingrino R, Kaukinen K, et al. Inflammatory processes have differential effects on claudins 2, 3 and 4 in colonic epithelial cells. Lab Invest. 2005;85:1139-1162.
52. Amasheh S, Milatz S, Krug SM, et al. Tight junction proteins as channel formers and barrier builders. Ann N Y Acad Sci. 2009;1165:211-219.
53. Suzuki T, Yoshinaga N, Tanabe S. Interleukin-6 (IL-6) regulates claudin-2 expression and tight junction permeability in intestinal epithelium. J Biol Chem. 2011;286:31263-31271.
54. Souza M, Cheetham SM, Azevedo MS, et al. Cytokine and antibody responses in gnotobiotic pigs after infection with human norovirus genogroup II.4 (HS66 strain). J Virol. 2007;81:9183-9192.
55. Lindesmith L, Moe C, Lependu J, et al. Cellular and humoral immunity following Snow Mountain virus challenge. J Virol. 2005;79: 2900-2909.